LETTERS
Emerging Human indiscriminately, and an expert commit- seum), some bacterial diseases (e.g., tee decided to abandon these two terms legionellosis), and protozoan (e.g., pri- Infectious Diseases: and recommended “zoonoses” as “dis- mary amebic meningoencephalitis). Anthroponoses, eases and infections which are naturally Intracellular parasites of animals (virus- transmitted between vertebrate animals es, rickettsiae, and chlamydiae) cannot Zoonoses, and and man” (3). A limited number of be sapronotic agents. The term “saprono- Sapronoses zoonotic agents can cause extensive out- sis” was introduced in epidemiology as a breaks; many zoonoses, however, attract useful concept (6–8). For these diseases To the Editor: The source of infection the public’s attention because of the high the expert committee applied the term has always been regarded as an utmost death rate associated with the infections. “sapro-zoonoses,” defined as “having factor in epidemiology. Human commu- In addition, zoonoses are sometimes con- both a vertebrate host and a nonanimal nicable diseases can be classified accord- tagious for hospital personnel (e.g., hem- developmental site or reservoir (organic ing to the source of infection as anthro- orrhagic fevers). Zoonotic diseases can matter, soil, and plants)” (3,9). However, ponoses (when the source is an infectious be classified according to the ecosystem the term sapronoses is more appropriate human; interhuman transfer is typical), in which they circulate. The classifica- because animals are not the source of zoonoses (the source is an infectious ani- tion is either synanthropic zoonoses, infection for humans. While anthro- mal; interhuman transfer is uncommon), with an urban (domestic) cycle in which ponoses and zoonoses are usually the and sapronoses (the source is an abiotic the source of infection are domestic and domains for professional activities of substrate, nonliving environment; inter- synanthropic animals (e.g., urban rabies, human and veterinary microbiologists, human transfer is exceptional). The cat scratch disease, and zoonotic ring- respectively, sapronoses may be the source of infection is often the reservoir worm) or exoanthropic zoonoses, with a domain for environmental microbiolo- or, in ecologic terms, the habitat where sylvatic (feral and wild) cycle in natural gists. The underdiagnosis rate for the etiologic agent of the disease normal- foci (4) outside human habitats (e.g., sapronoses is probably higher than that ly thrives, grows, and replicates. A char- arboviroses, wildlife rabies, Lyme dis- for anthroponoses and zoonoses, and an acteristic feature of most zoonoses and ease, and tularemia). However, some increase should be expected in both inci- sapronoses is that once transmitted to zoonoses can circulate in both urban and dence and number of sapronoses. humans, the epidemic chain is usually natural cycles (e.g., yellow fever and Legionellosis, Pontiac fever, nontubercu- aborted, but the clinical course might be Chagas disease). A number of zoonotic lous mycobacterioses, and primary ame- sometimes quite severe, even fatal. An agents are arthropod-borne (5); others bic meningoencephalitis are a few ecologic rule specifies that an obligatory are transmitted by direct contact, alimen- sapronoses that have emerged in the past parasite should not kill its host to benefit tary (foodborne and waterborne), or decade. In addition, the number of from the adapted long-term symbiosis, aerogenic (airborne) routes; and some opportunistic infections in immunosup- whereas an occasionally attacked alien are rodent-borne. pressed patients has grown markedly; host, such as a human, might be subject- Sapronoses (Greek “sapros” = decay- many of these diseases and some nosoco- ed to a severe disease or even killed rap- ing; “sapron” means in ecology a decay- mial infections are, in fact, also idly by the parasite because no evolu- ing organic substrate) are human dis- sapronoses. tionary adaptation to that host exists (1). eases transmissible from abiotic environ- As with any classification, grouping In this letter, only microbial infections ment (soil, water, decaying plants, or ani- human diseases in epidemiologic cate- are discussed; metazoan invasion and mal corpses, excreta, and other substra- gories according to the source of infec- infestations have been omitted. ta). The ability of the agent to grow tion has certain pitfalls. Some arthropod- Anthroponoses (Greek “anthrópos” = saprophytically and replicate in these borne diseases (urban yellow fever, man, “nosos” = disease) are diseases substrata (i.e., not only to survive or con- dengue, epidemic typhus, tickborne transmissible from human to human. taminate them secondarily) are the most relapsing fever, epidemic relapsing fever, Examples include rubella, smallpox, important characteristics of a sapronotic and malaria) might be regarded as diphtheria, gonorrhea, ringworm microbe. Sapronotic agents thus carry on anthroponoses rather than zoonoses (Trichophyton rubrum), and trichomoni- two diverse ways of life: saprophytic (in because the donor of the infectious blood asis. an abiotic substrate at ambient tempera- for the vector is an infected human and Zoonoses (Greek “zoon” = animal) are ture) and parasitic (pathogenic, at the not a vertebrate animal. However, the diseases transmissible from living ani- temperature of a homeotherm vertebrate human infection is caused by an (inverte- mals to humans (2). These diseases were host). Typical sapronoses are visceral brate) animal in which the agent repli- formerly called anthropozoonoses, and mycoses caused by dimorphic fungi cates, and the term zoonoses is preferred. the diseases transmissible from humans (e.g., coccidioidomycosis and histoplas- HIV is of simian origin with a sylvatic to animals were called zooanthro- mosis), “monomorphic” fungi (e.g., cycling among wild primates and acci- ponoses. Unfortunately, many scientists aspergillosis and cryptococcosis), certain dental infection of humans who hunted used these terms in the reverse sense or superficial mycoses (Microsporum gyp- or ate them; the human disease (AIDS)
Emerging Infectious Diseases • Vol. 9, No. 3, March 2003 403 LETTERS might thus have been regarded as a 4. Pavlovsky EN. Natural nidality of trans- other regions of the world, especially in zoonosis in the very first phase but later missible diseases. Urbana (IL): Southeast Asia, low-level resistance to has spread in the human population as a University of Illinois Press; 1966. fluoroquinolones in Shigella spp. has typical anthroponosis and caused the 5. Beaty BJ, Marquardt WC, editors. The been observed for some time (4,5). present pandemic. Similarly, pandemic biology of disease vectors. Niwot (CO): After a lapse of almost 14 years, clus- University Press of Colorado; 1996. strains of influenza developed through an ters of patients with acute bacillary 6. Terskikh VI. Diseases of humans and ani- antigenic shift from avian influenza A mals caused by microbes able to repro- dysentery were seen at the subdivisional viruses. For some etiologic agents or duce in an abiotic environment that repre- hospital, Diamond Harbour, in eastern their genotypes, both animals and sents their living habitat (in Russian). India. No cases of dysentery had been humans are concurrent reservoirs (hepa- Zhurn Mikrobiol Epidemiol Immunobiol reported during the comparable period in titis virus E, Norwalk-like calicivirus, (Moscow) 1958;8:118–22. previous years. A total of 1,124 case- enteropathogenic Escherichia coli, 7. Somov GP, Litvin VJ. Saprophytism and patients were admitted from March Pneumocystis, Cryptosporidium, Giar- parasitism of pathogenic bacteria—eco- through June 2002. The startling feature dia, and Cyclospora); these diseases logical aspects (in Russian). Novosibirsk: of these infections was their unrespon- might conditionally be called anthropo- Nauka; 1988. siveness to even the newer fluoro- zoonoses. Other difficulties can occur 8. Krauss H, Weber A, Enders B, Schiefer quinolones such as norfloxacin and HG, Slenczka W, Zahner H. Zoonosen, 2. with classifying diseases caused by ciprofloxacin, the drugs often used to Aufl. Köln: Deutscher Ärzte-Verlag; sporulating bacteria (Clostridium and 1997. treat shigellosis. Clinicians tried various Bacillus): Their infective spores survive 9. Schwabe CV. Veterinary medicine and antibiotics, mostly in combinations, in the soil or in other substrata for very human health. Baltimore: Williams & without benefit. Clinicians also random- long periods, though they are usually pro- Wilkins; 1964. ly used anti-amoebic drugs without suc- duced after a vegetative growth in the abi- cess. otic environment, which can include ani- Address for correspondence: Zdenek Hubálek, An investigating team collected nine mal carcasses. These diseases should Institute of Vertebrate Biology, Academy of fresh fecal samples from dysentery therefore be called sapronoses. For some Sciences, Klásterní 2, CZ-69142 Valtice, Czech patients admitted to this hospital; 4 other etiologic agents, both animals and Republic; fax: 420-519352387; e-mail: zhubalek@ (44%) yielded S. dysenteriae type 1 on brno.cas.cz abiotic environment can be the reservoir culture. For isolation of Shigella spp., (Listeria, Erysipelothrix, Yersinia pseudo- stool samples were inoculated into tuberculosis, Burkholderia pseudomallei, MacConkey agar and Hektoen Enteric and Rhodococcus equi), and the diseases agar (Difco, Detroit, MI), and the charac- might be, in fact, called saprozoonosis Multidrug-Resistant teristic colonies were identified by stan- (not sensu 9 ) in that their source can be dard biochemical methods (6). either an animal or an abiotic substrate. Shigella dysenteriae Subsequently, serogroups and serotypes For a concise list of anthropo-, zoo-, Type 1: Forerunners were determined by visual inspection of and sapronoses, see the online appendix slide agglutination tests with commercial available from: URL: http://www. of a New Epidemic antisera (Denka Seiken, Tokyo). cdc.gov/ncidod/EID/vol9no3/02-0208- Strain in Eastern Antimicrobial susceptibility testing was app.htm. performed by an agar diffusion disk India? method, as recommended by the Zdenek Hubálek* To the Editor: Multidrug-resistant National Committee for Clinical *Academy of Sciences, Brno, Czech Republic Shigella dysenteriae type 1 caused an Laboratory Standards (7). Results extensive epidemic of shigellosis in east- showed that the organisms were resistant References ern India in 1984 (1). These strains were, to all commonly used antibiotics, includ- however, sensitive to nalidixic acid, and ing the fluoroquinolones (norfloxacin 1. Lederberg J. Infectious disease as an evo- and ciprofloxacin) but were sensitive to lutionary paradigm. Emerg Infect Dis clinicians found excellent results by ofloxacin. On our advice, the clinicians 1997;3:417–23. using it to treat bacillary dysentery cases. 2. Bell JC, Palmer SR, Payne JM. The Subsequently, in 1988 in Tripura, an used ofloxacin with good results. zoonoses (infections transmitted from eastern Indian state, a similar outbreak of A similar outbreak of S. dysenteriae animals to man). London: Arnold; 1988. shigellosis occurred in which the isolated type 1 occurred in the northern part of 3. World Health Organization. Joint strains of S. dysenteriae type 1 were even West Bengal in eastern India among tea WHO/FAO expert committee on resistant to nalidixic acid (2). Since then, garden laborers from April 2002 to May zoonoses. 2nd report. WHO technical few cases of shigellosis have occurred in 2002; 1,728 persons were affected report series no. 169, Geneva; 1959. 3rd this region, and S. dysenteriae type 1 (attack rate of 25.6%). Sixteen persons report, WHO Technical Report Series no. strains are scarcely encountered (3). In died. The isolated S. dysenteriae type 1 378, Geneva; The Organization; 1967. strains were found intermediately sensi-
404 Emerging Infectious Diseases • Vol. 9, No. 3, March 2003 CDC - Emerging Human Infectious Diseases: Anthroponoses, Zoonoses, and Sapronoses Appendix: Important Anthroponoses, Zoonoses, and Sapronoses1
Anthroponoses
Measles*; rubella; mumps; influenza; common cold; viral hepatitis; poliomyelitis; AIDS*; infectious mononucleosis; herpes simplex; smallpox; trachoma; chlamydial pneumonia and cardiovascular disease*; mycoplasmal infections*; typhoid fever; cholera; peptic ulcer disease*; pneumococcal pneumonia; invasive group A streptococcal infections; vancomycin-resistant enterococcal disease*; meningococcal disease*; whooping cough*; diphtheria*; Haemophilus infections* (including Brazilian purpuric fever*); syphilis; gonorrhea; tuberculosis* (multidrug- resistant strains); candidiasis*; ringworm (Trichophyton rubrum); Pneumocystis pneumonia* (human genotype); microsporidial infections*; cryptosporidiosis* (human genotype); giardiasis* (human genotype); amebiasis; and trichomoniasis.
Zoonoses Transmitted by Direct Contact, Alimentary (Foodborne and Waterborne), or Aerogenic (Airborne) Routes
Rabies; hemorrhagic fever with renal syndrome*; hantavirus pulmonary syndrome*; Venezuelan*; Brazilian*; Argentinian and Bolivian hemorrhagic fevers; Lassa; Marburg; and Ebola hemorrhagic fevers*; Hendra and Nipah hemorrhagic bronchopneumonia*; hepatitis E*; herpesvirus simiae B infection; human monkeypox*;Q fever; sennetsu fever; cat scratch disease; psittacosis; mammalian chlamydiosis*; leptospirosis; zoonotic streptococcosis; listeriosis; erysipeloid; campylobacterosis*; salmonellosis*; hemorrhagic colitis*; hemolytic uremic syndrome*; yersiniosis; pseudotuberculosis; sodoku; Haverhill fever; brucellosis*; tularemia*; glanders; bovine and avian tuberculosis*; zoonotic ringworm; toxoplasmosis; and cryptosporidiosis* (calf genotype 2).
Zoonoses Transmitted by Hematophagous Arthropods
Hard ticks (Ixodidae)
Russian spring-summer encephalitis; Central European encephalitis; louping ill; Kyasanur Forest disease; Powassan; Crimean-Congo hemorrhagic fever*; Colorado tick fever; Rocky Mountain spotted fever; boutonneuse fever; African tick typhus*; other rickettsial fevers*; human granulocytic ehrlichiosis*; Lyme disease*; tularemia; and babesiosis.
Soft ticks (Argasidae)
Tickborne relapsing fever
Mites (Trombiculidae, Dermanyssidae)
Scrub typhus; rickettsialpox
Lice (Anoplura)
Epidemic typhus; trench fever*; and epidemic relapsing fever http://www.cdc.gov/ncidod/EID/vol9no3/02-0208-app.htm[7/26/2010 4:55:29 PM] CDC - Emerging Human Infectious Diseases: Anthroponoses, Zoonoses, and Sapronoses
Triatomine Bugs (Triatominae)
Chagas disease
Sandflies (Phlebotominae)
Sandfly fever; vesicular stomatitis; Oroya fever; and leishmaniasis
Mosquitoes (Culicidae)
Eastern; Western; and Venezuelan equine encephalomyelitis; Sindbis fever; Chikungunya and O’nyong nyong fevers*; Ross River epidemic polyarthritis*; Japanese encephalitis*; West Nile fever*; St. Louis encephalitis; yellow fever; dengue/dengue hemorrhagic fever*; Murray Valley encephalitis; California encephalitis; Rift Valley fever*; and malaria*
Biting Midges (Ceratopogonidae)
Oropouche fever; vesicular stomatitis
Tsetse-flies (Glossinidae)
African trypanosomiasis
Fleas (Siphonaptera)
Murine typhus*; cat-scratch fever*; plague
Sapronoses
Chlamydia-like pneumonia* (amoebic endosymbionts Parachlamydia acanthamoebae and other Parachlamydiaceae); tetanus; gas gangrene (Clostridium perfringens; C. septicum; C. novyi); intestinal clostridiosis* (C. difficile; C. perfringens); botulism; food poisoning* (Bacillus cereus); anthrax; vibrio gastroenteritis* or dermatitis (Vibrio parahaemolyticus; V. vulnificus); nosocomial Klebsiella pneumoniae and Pseudomonas aeruginosa bacteremia* (including antibiotic-resistant strains); bacterial infections associated with cystic fibrosis* (Burkholderia cepacia; Ralstonia spp.); melioidosis* (B. pseudomallei); legionellosis* and Pontiac fever* (Legionella pneumophila; L. micdadei; and other spp.); atypical bacterial meningitis and sepsis* (Chryseobacterium meningosepticum); acinetobacter bacteremia* (Acinetobacter calcoaceticus; A. baumannii; A. radioresistens); corynebacterial endocarditis* (Corynebacterium serosis; C. amycolatum and other nondiphtheriae corynebacteria); rhodococcosis* (Rhodococcus equi); possibly leprosy (some strains of Mycobacterium leprae were detected as living saprophytically in wet moss habitats); Buruli ulcer disease* (M. ulcerans); mycobacterial diseases other than tuberculosis* (M. kansasii; M. xenopi; M. marinum; M. haemophilum; M. fortuitum; M. scrofulaceum; M. abscessus; and other spp.); nocardiosis (Nocardia asteroides; N. brasiliensis); actinomycetom (Actinomadura madurae; A. pelletieri; Streptomyces somaliensis); dermatophytosis (Microsporum gypseum); histoplasmosis* http://www.cdc.gov/ncidod/EID/vol9no3/02-0208-app.htm[7/26/2010 4:55:29 PM] CDC - Emerging Human Infectious Diseases: Anthroponoses, Zoonoses, and Sapronoses (Histoplasma capsulatum; H. duboisii); blastomycosis (Blastomyces dermatitidis); emmonsiosis (Emmonsia crescens; E. parva); paracoccidioidomycosis (Paracoccidioides brasiliensis); coccidioidomycosis* (Coccidioides immitis); sporotrichosis (Sporothrix schenckii); cryptococcosis* (Cryptococcus neoformans); aspergillosis (Aspergillus fumigatus); mucormycosis (Absidia corymbifera and some other Mucorales); entomophthoromycosis (Basidiobolus; Conidiobolus; and Entomophthora spp.); maduromycetom (Madurella mycetomatis; M. grisea; Pseudoallescheria boydii; Leptosphaeria senegalensis; Neotestudina rosatii); chromoblastomycosis (Phialophora verrucosa; Exophiala jeanselmei; Fonsecaea compacta; F. pedrosoi; Cladosporium carionii; Rhinocladiella aquaspersa); phaeohyphomycosis (Wangiella dermatitidis; Dactylaria gallopava; Exophiala spinifera); fusariosis* (Fusarium oxysporum; F. solani); primary amebic meningoencephalitis* (Naegleria fowleri); and amoebic keratitis or chronic granulomatous amoebic meningoencephalitis* (Acanthamoeba castellanii; A. polyphaga).
1 Emerging and reemerging diseases are marked with an asterisk.
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